The plant axis as the command centre for (re)distribution of sucrose and amino acids

Abstract

Along with the increase in size required for optimal colonization of terrestrial niches, channels for bidirectional bulk transport of materials in land plants evolved during a period of about 100 million years. These transport systems are essentially still in operation - though perfected over the following 400 million years - and make use of hydrostatic differentials. Substances are accumulated or released at the loading and unloading ends, respectively, of the transport channels. The intermediate stretch between the channel termini is bifunctional and executes orchestrated release and retrieval of solutes. Analyses of anatomical and physiological data demonstrate that the release/retrieval zone extends deeper into sources and sinks than is commonly thought and covers usually much more than 99% of the translocation stretch. This review sketches the significance of events in the intermediate stretch for distribution of organic materials over the plant body. Net leakage from the channels does not only serve maintenance and growth of tissues along the pathway, but also diurnal, short-term or seasonal storage of reserve materials, and balanced distribution of organic C- and N-compounds over axial and terminal sinks. Release and retrieval are controlled by plasma-membrane transporters at the vessel/parenchyma interface in the contact pits along xylem vessels and by plasma-membrane transporters at the interface between companion cells and phloem parenchyma along sieve tubes. The xylem-to-phloem pathway vice versa is a bifacial, radially oriented system comprising a symplasmic pathway, of which entrance and exit are controlled at specific membrane checkpoints, and a parallel apoplasmic pathway. A broad range of specific sucrose and amino-acid transporters are deployed at the checkpoint plasma membranes. SUCs, SUTs, STPs, SWEETs, and AAPs, LTHs, CATs are localized to the plasma membranes in question, both in monocots and eudicots. Presence of Umamits in monocots is uncertain. There is some evidence for endo- and exocytosis at the vessel/parenchyma interface supplementary to the transporter-mediated uptake and release. Actions of transporters at the checkpoints are equally decisive for storage and distribution of amino acids and sucrose in monocots and eudicots, but storage and distribution patterns may differ between both taxa. While the majority of reserves is sequestered in vascular parenchyma cells in dicots, lack of space in monocot vasculature urges "outsourcing" of storage in ground parenchyma around the translocation path. In perennial dicots, specialized radial pathways (rays) include the sites for seasonal alternation of storage and mobilization. In dicots, apoplasmic phloem loading and a correlated low rate of release along the path would favour supply with photoassimilates of terminal sinks, while symplasmic phloem loading and a correlated higher rate of release along the path favours supply of axial sinks and transfer to the xylem. The balance between the resource acquisition by terminal and axial sinks is an important determinant of relative growth rate and, hence, for the fitness of plants in various habitats. Body enlargement as the evolutionary drive for emergence of vascular systems and mass transport propelled by hydrostatic differentials.

Keywords: Amino acid transporters; C-Allocation; N-Allocation; Radial xylem-to-phloem transfer v.v.; Rays; Sieve tubes; Sucrose transporters; Vessel contact cells; Xylem vessels.